Cell-Based Drug Delivery Systems with Innate Homing Capability as a Novel Nanocarrier Platform

References

• Allen TM, Culllis PR. Drug delivery systems: entering the mainstream. Science. 2004;303(5665):1818–1822.
   PubMed Web of Science ®Google Scholar
• Vargason AM, Anselmo AC, Mitragotri S. The evolution of commercial drug delivery technologies. Nat Biomed Eng. 2021;5(9):951–967.
   PubMed Web of Science ®Google Scholar
• Chi J, Ma Q, Shen Z, et al. Targeted nanocarriers based on iodinated-cyanine dyes as immunomodulators for synergistic phototherapy. Nanoscale. 2020;12(20):11008–11025.
   PubMed Web of Science ®Google Scholar
• Kolluru LP, Rizvi SA, D’Souza M, D’Souza MJ. Formulation development of albumin based theragnostic nanoparticles as a potential delivery system for tumor targeting. J Drug Target. 2013;21(1):77–86.
   PubMed Web of Science ®Google Scholar
• Hosseinidoust Z, Mostaghaci B, Yasa O, Park BW, Singh AV, Sitti M. Bioengineered and biohybrid bacteria-based systems for drug delivery. Adv Drug Deliv Rev. 2016;106(Pt A):27–44.
   PubMedGoogle Scholar
• Ma Y, Nolte RJ, Cornelissen JJ. Virus-based nanocarriers for drug delivery. Adv Drug Deliv Rev. 2012;64(9):811–825.
   PubMed Web of Science ®Google Scholar
• Li J, Zhao J, Tan T, et al. Nanoparticle drug delivery system for glioma and its efficacy improvement strategies: a comprehensive review. Int J Nanomedicine. 2020;15:2563–2582.
   PubMed Web of Science ®Google Scholar
• Wu Y, Liu Y, Wang T, Jiang Q, Xu F, Liu Z. Living cell for drug delivery. Eng Regen. 2022;3(2):131–148.
   Google Scholar
• Moon JJ, Huang B, Irvine DJ. Engineering nano- and microparticles to tune immunity. Adv Mater. 2012;24(28):3724–3746.
   PubMed Web of Science ®Google Scholar
• Hu CM, Fang RH, Zhang L. Erythrocyte-inspired delivery systems. Adv Healthc Mater. 2012;1(5):537–547.
   PubMed Web of Science ®Google Scholar
• Bhateria M, Rachumallu R, Singh R, Bhatta RS. Erythrocytes-based synthetic delivery systems: transition from conventional to novel engineering strategies. Expert Opin Drug Deliv. 2014;11(8):1219–1236.
   PubMed Web of Science ®Google Scholar
• Brahler M, Georgieva R, Buske N, et al. Magnetite-loaded carrier erythrocytes as contrast agents for magnetic resonance imaging. Nano Lett. 2006;6(11):2505–2509.
   PubMed Web of Science ®Google Scholar
• Villa CH, Anselmo AC, Mitragotri S, Muzykantov V. Red blood cells: supercarriers for drugs, biologicals, and nanoparticles and inspiration for advanced delivery systems. Adv Drug Deliv Rev. 2016;106(Pt A):88–103.
   PubMedGoogle Scholar
• Fraternale A, Casabianca A, Rossi L, et al. Erythrocytes as carriers of reduced glutathione (GSH) in the treatment of retroviral infections. J Antimicrob Chemother. 2003;52(4):551–554.
   PubMed Web of Science ®Google Scholar
• Bossa F, Annese V, Valvano MR, et al. Erythrocytes-mediated delivery of dexamethasone 21-phosphate in steroid-dependent ulcerative colitis: a randomized, double-blind Sham-controlled study. Inflamm Bowel Dis. 2013;19(9):1872–1879.
   PubMed Web of Science ®Google Scholar
• Kontos S, Kourtos IC, Dane KY, Hubbell JA. Engineering antigens for in situ erythrocyte binding induces T-cell deletion. Proc Natl Acad Sci U S A. 2013;110(1):E60–E68.
   PubMed Web of Science ®Google Scholar
• Phua KK, Boczkowski D, Dannull J, Pruitt S, Leong KW, Nair SK. Whole blood cells loaded with messenger RNA as an anti-tumor vaccine. Adv Healthc Mater. 2014;3(6):837–842.
   PubMed Web of Science ®Google Scholar
• Pishesha N, Bilate AM, Wibowo MC, et al. Engineered erythrocytes covalently linked to antigenic peptides can protect against autoimmune disease. Proc Natl Acad Sci U S A. 2017;114(12):3157–3162.
   PubMed Web of Science ®Google Scholar
• Ihler GM, Glew RH, Schnure FW. Enzyme loading of erythrocytes. Proc Natl Acad Sci U S A. 1973;70(9):2663–2666.
   PubMed Web of Science ®Google Scholar
• Koleva L, Bovt E, Ataullakhanov F, Sinauridze E. Erythrocytes as carriers: from drug delivery to biosensors. Pharmaceutics. 2020;12(3):276.
   PubMed Web of Science ®Google Scholar
• Li Y, Raza F, Liu Y, et al. Clinical progress and advanced research of red blood cells based drug delivery system. Biomaterials. 2021;279:121202.
   PubMed Web of Science ®Google Scholar
• Semple JW, Italiano JE, Freedman J. Platelets and the immune continuum. Nat Rev Immunol. 2011;11(4):264–274.
   PubMed Web of Science ®Google Scholar
• Wang H, Wu J, Williams GR, et al. Platelet-membrane-biomimetic nanoparticles for targeted antitumor drug delivery. J Nanobiotechnology. 2019;17(1):60.
   PubMedGoogle Scholar
• Buergy D, Wenz F, Groden C, Brockman MA. Tumor-platelet interaction in solid tumors. Int J Cancer. 2012;130(12):2747–2760.
   PubMed Web of Science ®Google Scholar
• Borsig L. The role of platelet activation in tumor metastasis. Expert Rev Anticancer Ther. 2008;8(8):1247–1255.
   PubMed Web of Science ®Google Scholar
• Mitragotri S, Burke PA, Langer R. Overcoming the challenges in administering biopharmaceuticals: formulation and delivery strategies. Nat Rev Drug Discov. 2014;13(9):655–672.
   PubMed Web of Science ®Google Scholar
• Albarran B, Hoffman AS, Stayton PS. Efficient intracellular delivery of a pro-apoptotic peptide with A pH-responsive carrier. React Funct Polym. 2011;71(3):261–265.
   PubMed Web of Science ®Google Scholar
• Larochelle C, Alvarez JI, Prat A. How do immune cells overcome the blood-brain barrier in multiple sclerosis? FEBS Lett. 2011;585(23):3770–3780.
   PubMed Web of Science ®Google Scholar
• Varatharaj A, Galea I. The blood-brain barrier in systemic inflammation. Brain Behav Immun. 2017;60:1–12.
   PubMed Web of Science ®Google Scholar
• Zhang W, Wang M, Tang W, et al. Nanoparticle-laden macrophages for tumor-tropic drug delivery. Adv Mater. 2018;30(50):e1805557.
   PubMed Web of Science ®Google Scholar
• Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013;13(3):159–175.
   PubMed Web of Science ®Google Scholar
• Kitamura T, Qian BZ, Pollard JW. Immune cell promotion of metastasis. Nat Rev Immunol. 2015;15(2):73–86.
   PubMed Web of Science ®Google Scholar
• Smith JA. Neutrophils, host defense, and inflammation: a double-edged sword. J Leukoc Biol. 1994;56(6):672–686.
   PubMed Web of Science ®Google Scholar
• Chu D, Gao J, Wang Z. Neutrophil-mediated delivery of therapeutic nanoparticles across blood vessel barrier for treatment of inflammation and infection. ACS nano. 2015;9(12):11800–11811.
   PubMed Web of Science ®Google Scholar
• De Bondt M, Hellings N, Opdenakker G, Struyf S. Neutrophils: underestimated players in the pathogenesis of multiple sclerosis (MS). Int J Mol Sci. 2020;21(12):4558.
   PubMed Web of Science ®Google Scholar
• Dong Y, Lagarde J, Xicota L, et al. Neutrophil hyperactivation correlates with Alzheimer’s disease progression. Ann Neurol. 2018;83(2):387–405.
   PubMed Web of Science ®Google Scholar
• Price CJ, Menon DK, Peters AM, et al. Cerebral neutrophil recruitment, histology, and outcome in acute ischemic stroke: an imaging-based study. Stroke. 2004;35(7):1659–1664.
   PubMed Web of Science ®Google Scholar
• Jickling GC, Liu D, Ander BP, Stamova B, Zhan X, Sharp FR. Targeting neutrophils in ischemic stroke: translational insights from experimental studies. J Cereb Blood Flow Metab. 2015;35(6):888–901.
   PubMed Web of Science ®Google Scholar
• Szmydynger-Chodobska J, Strazielle N, Zink BJ, Ghersi-Egea JF, Chodobski A. The role of the choroid plexus in neutrophil invasion after traumatic brain injury. J Cereb Blood Flow Metab. 2009;29(9):1503–1516.
   PubMed Web of Science ®Google Scholar
• Clark RS, Schiding JK, Kaczorowski SL, Marion DW, Kochanek PM. Neutrophil accumulation after traumatic brain injury in rats: comparison of weight drop and controlled cortical impact models. J Neurotrauma. 1994;11(5):499–506.
   PubMed Web of Science ®Google Scholar
• Aizik G, Grad E, Golomb G. Monocyte-mediated drug delivery systems for the treatment of cardiovascular diseases. Drug Deliv Transl Res. 2018;8(4):868–882.
   PubMed Web of Science ®Google Scholar
• Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K. Development of monocytes, macrophages, and dendritic cells. Science. 2010;327(5966):656–661.
   PubMed Web of Science ®Google Scholar
• Smith BR, Ghosn EE, Rallapalli H, et al. Selective uptake of single-walled carbon nanotubes by circulating monocytes for enhanced tumour delivery. Nat Nanotechnol. 2014;9(6):481–487.
   PubMed Web of Science ®Google Scholar
• Serhan CN, Ward PA, Gilroy DW. Fundamentals of Inflammation. Cambridge University Press; 2010.
   Google Scholar
• Kapellos TS, Taylor L, Lee H, et al. A novel real time imaging platform to quantify macrophage phagocytosis. Biochem Pharmacol. 2016;116:107–119.
   PubMed Web of Science ®Google Scholar
• Hirayama D, Iida T, Nakase H. The phagocytic function of macrophage-enforcing innate immunity and tissue homeostasis. Int J Mol Sci. 2017;19(1):92.
   PubMed Web of Science ®Google Scholar
• Dong X, Chu D, Wang Z. Leukocyte-mediated delivery of nanotherapeutics in inflammatory and tumor sites. Theranostics. 2017;7(3):751–763.
   PubMed Web of Science ®Google Scholar
• Anand RJ, Kohler JW, Cavallo JA, Li J, Dubowski T, Hackam DJ. Toll-like receptor 4 plays a role in macrophage phagocytosis during peritoneal sepsis. J Pediatr Surg. 2007;42(6):927–932.
   PubMed Web of Science ®Google Scholar
• Torres FG, Troncoso OP, Pisani A, Gatto F, Bardi G. Natural polysaccharide nanomaterials: an overview of their immunological properties. Int J Mol Sci. 2019;20(20):5092.
   PubMed Web of Science ®Google Scholar
• Suits AG, Chait A, Aviram M, Heinecke JW. Phagocytosis of aggregated lipoprotein by macrophages: low density lipoprotein receptor-dependent foam-cell formation. Proc Natl Acad Sci U S A. 1989;86(8):2713–2717.
   PubMed Web of Science ®Google Scholar
• Yousefpour P, Chikoti A. Co-opting biology to deliver drugs. Biotechnol Bioeng. 2014;111(9):1699–1716.
   PubMed Web of Science ®Google Scholar
• Lewis C, Murdoch C. Macrophage responses to hypoxia: implications for tumor progression and anti-cancer therapies. Am J Pathol. 2005;167(3):627–635.
   PubMed Web of Science ®Google Scholar
• Klimp AH, De Vries EG, Scherphof GL, Daemen T. A potential role of macrophage activation in the treatment of cancer. Crit Rev Oncol Hematol. 2002;44(2):143–161.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Haney MJ, Mahajan V, et al. Active targeted macrophage-mediated delivery of catalase to affected brain regions in models of parkinson’s disease. J Nanomed Nanotechnol. 2011;S4:003.
   PubMedGoogle Scholar
• Yoo JW, Irvine DJ, Discher DE, Mitragotri S. Bio-inspired, bioengineered and biomimetic drug delivery carriers. Nat Rev Drug Discov. 2011;10(7):521–535.
   PubMed Web of Science ®Google Scholar
• Ma Q, Cao J, Gao Y, et al. Microfluidic-mediated nano-drug delivery systems: from fundamentals to fabrication for advanced therapeutic applications. Nanoscale. 2020;12(29):15512–15527.
   PubMed Web of Science ®Google Scholar
• Jones RB, Mueller S, Kumari S, et al. Antigen recognition-triggered drug delivery mediated by nanocapsule-functionalized cytotoxic T-cells. Biomaterials. 2017;117:44–53.
   PubMed Web of Science ®Google Scholar
• Lanzavecchia A, Iezzi G, Viola A. From TCR engagement to T cell activation: a kinetic view of T cell behavior. Cell. 1999;96(1):1–4.
   PubMed Web of Science ®Google Scholar
• Singh N, Lee YG, Shestova O, et al. Impaired death receptor signaling in leukemia causes antigen-independent resistance by inducing CAR T-cell dysfunction. Cancer Discov. 2020;10(4):552–567.
   PubMed Web of Science ®Google Scholar
• Ivica NA, Young CM. Tracking the CAR-T revolution: analysis of clinical trials of CAR-T and TCR-T therapies for the treatment of cancer (1997–2020). Healthcare. 2021;9(8):1062.
   Web of Science ®Google Scholar
• Sterner RC, Sterner RM. CAR-T cell therapy: current limitations and potential strategies. Blood Cancer J. 2021;11(4):69.
   PubMed Web of Science ®Google Scholar
• Siriwon N, Kim YJ, Siegler E, et al. CAR-T cells surface-engineered with drug-encapsulated nanoparticles can ameliorate intratumoral T-cell hypofunction. Cancer Immunol Res. 2018;6(7):812–824.
   PubMed Web of Science ®Google Scholar
• Jin C, Fotaki G, Ramachandran M, Nilsson B, Essand M, Yu D. Safe engineering of CAR T cells for adoptive cell therapy of cancer using long-term episomal gene transfer. EMBO Mol Med. 2016;8(7):702–711.
   PubMed Web of Science ®Google Scholar
• Park TS, Rosenberg SA, Morgan RA. Treating cancer with genetically engineered T cells. Trends Biotechnol. 2011;29(11):550–557.
   PubMed Web of Science ®Google Scholar
• Bald T, Krummel MF, Smyth MJ, Barry KC. The NK cell-cancer cycle: advances and new challenges in NK cell-based immunotherapies. Nat Immunol. 2020;21(8):835–847.
   PubMed Web of Science ®Google Scholar
• Myers JA, Miller JS. Exploring the NK cell platform for cancer immunotherapy. Nat Rev Clin Oncol. 2021;18(2):85–100.
   PubMed Web of Science ®Google Scholar
• Smyth MJ, Cretney E, Kelly JM, et al. Activation of NK cell cytotoxicity. Mol Immunol. 2005;42(4):501–510.
   PubMed Web of Science ®Google Scholar
• Wang W, Erbe AK, Hank JA, Morris ZS, Sondel PM. NK cell-mediated antibody-dependent cellular cytotoxicity in cancer immunotherapy. Front Immunol. 2015;6:368.
   PubMed Web of Science ®Google Scholar
• Martinet L, Smyth MJ. Balancing natural killer cell activation through paired receptors. Nat Rev Immunol. 2015;15(4):243–254.
   PubMed Web of Science ®Google Scholar
• Deng G, Sun Z, Li S, et al. Cell-membrane immunotherapy based on natural killer cell membrane coated nanoparticles for the effective inhibition of primary and abscopal tumor growth. ACS Nano. 2018;12(12):12096–12108.
   PubMed Web of Science ®Google Scholar
• Vitale M, Cantoni C, Pietra G, Mingari MC, Moretta L. Effect of tumor cells and tumor microenvironment on NK-cell function. Eur J Immunol. 2014;44(6):1582–1592.
   PubMed Web of Science ®Google Scholar
• Zhang C, Burger MC, Jennewein L, et al. ErbB2/HER2-specific NK cells for targeted therapy of glioblastoma. J Natl Cancer Inst. 2015;108:5.
   Google Scholar
• Valipour B, Velaei K, Abedelahi A, Karimipour M, Darabi M, Charoudeh HN. NK cells: an attractive candidate for cancer therapy. J Cell Physiol. 2019;234(11):19352–19365.
   PubMed Web of Science ®Google Scholar
• Su Y, Xie Z, Kim GB, Dong C, Yang J. Design strategies and applications of circulating cell-mediated drug delivery systems. ACS Biomater Sci Eng. 2015;1(4):201–217.
   PubMed Web of Science ®Google Scholar
• Teng CF, Jeng LB, Shyu WC. Role of insulin-like growth factor 1 receptor signaling in stem cell stemness and therapeutic efficacy. Cell Transplant. 2018;27(9):1313–1319.
   PubMed Web of Science ®Google Scholar
• Mills KM, Szczerkowski JLA, Habib SJ. Wnt ligand presentation and reception: from the stem cell niche to tissue engineering. Open Biol. 2017;7(8):170140.
   PubMed Web of Science ®Google Scholar
• Han Y, Li X, Zhang Y, Han Y, Chang F, Ding J. Mesenchymal stem cells for regenerative medicine. Cells. 2019;8(8):886.
   PubMed Web of Science ®Google Scholar
• Kolios G, Moodley Y. Introduction to stem cells and regenerative medicine. Respiration. 2013;85(1):3–10.
   PubMed Web of Science ®Google Scholar
• Tang J, Wang J, Huang K, et al. Cardiac cell-integrated microneedle patch for treating myocardial infarction. Sci Adv. 2018;4(11):eaat9365.
   PubMed Web of Science ®Google Scholar
• Salehi H, Al-Arag S, Middendorp E, Gergely C, Cuisinier F, Orti V. Dental pulp stem cells used to deliver the anticancer drug paclitaxel. Stem Cell Res Ther. 2018;9(1):103.
   PubMedGoogle Scholar
• Fu H, Wu Y, Yang X, et al. Stem cell and its derivatives as drug delivery vehicles: an effective new strategy of drug delivery system. AllLife. 2021;14(1):782–798.
   Google Scholar
• Xie C, Yang Z, Suo Y, et al. Systemically infused mesenchymal stem cells show different homing profiles in healthy and tumor mouse models. Stem Cells Transl Med. 2017;6(4):1120–1131.
   PubMed Web of Science ®Google Scholar
• Kean TJ, Lin P, Caplan AI, Dennis JE. MSCs: delivery routes and engraftment, cell-targeting strategies, and immune modulation. Stem Cells Int. 2013;2013:732742.
   PubMed Web of Science ®Google Scholar
• Xia J, Tsai AC, Cheng W, Yuan X, Ma T, Guan J. Development of a microdevice-based human mesenchymal stem cell-mediated drug delivery system. Biomater Sci. 2019;7(6):2348–2357.
   PubMed Web of Science ®Google Scholar
• Wang X, Chen H, Zeng X, et al. Efficient lung cancer-targeted drug delivery via a nanoparticle/MSC system. Acta Pharm Sin B. 2019;9(1):167–176.
   PubMed Web of Science ®Google Scholar
• Wang X, Gao J, Ouyang X, Wang J, Sun X, Lv Y. Mesenchymal stem cells loaded with paclitaxel-poly (lactic- co-glycolic acid) nanoparticles for glioma-targeting therapy. Int J Nanomedicine. 2018;13:5231–5248.
   PubMed Web of Science ®Google Scholar
• Hu Q, Sun W, Wang J, et al. Conjugation of haematopoietic stem cells and platelets decorated with anti-PD-1 antibodies augments anti-leukaemia efficacy. Nat Biomed Eng. 2018;2(11):831–840.
   PubMed Web of Science ®Google Scholar
• Su Y, Zhang T, Huang T, Gao J. Current advances and challenges of mesenchymal stem cells-based drug delivery system and their improvements. Int J Pharm. 2021;600:120477.
   PubMedGoogle Scholar
• Idorn M, Skadborg SK, Kellermann L, et al. Chemokine receptor engineering of T cells with CXCR2 improves homing towards subcutaneous human melanomas in xenograft mouse model. Oncoimmunology. 2018;7(8):e1450715.
   PubMed Web of Science ®Google Scholar
• D’souza N, Burns JS, Grisendi G, et al. MSC and tumors: homing, differentiation, and secretion influence therapeutic potential. Adv Biochem Eng Biotechnol. 2013;130:209–266.
   PubMed Web of Science ®Google Scholar
• Carlos TM, Harlan JM. Leukocyte-endothelial adhesion molecules. Blood. 1994;84(7):2068–2101.
   PubMed Web of Science ®Google Scholar
• Krueger TEG, Thorek DLJ, Denmeade SR, Isaacs JT, Brennen WN. Concise review: mesenchymal stem cell-based drug delivery: the good, the bad, the ugly, and the promise. Stem Cells Transl Med. 2018;7(9):651–663.
   PubMed Web of Science ®Google Scholar
• Tiet P, Berlin JM. Exploiting homing abilities of cell carriers: targeted delivery of nanoparticles for cancer therapy. Biochem Pharmacol. 2017;145:18–26.
   PubMed Web of Science ®Google Scholar
• Summers C, Rankin SM, Condliffe AM, Singh N, Peters AM, Chilvers ER. Neutrophil kinetics in health and disease. Trends Immunol. 2010;31(8):318–324.
   PubMed Web of Science ®Google Scholar
• Strieter RM, Lukacs NW, Standiford TJ, Kunkel SL. Cytokines. 2. Cytokines and lung inflammation: mechanisms of neutrophil recruitment to the lung. Thorax. 1993;48(7):765–769.
   PubMed Web of Science ®Google Scholar
• Phillipson M, Kubes P. The neutrophil in vascular inflammation. Nat Med. 2011;17(11):1381–1390.
   PubMed Web of Science ®Google Scholar
• Zarbock A, Ley K, McEver RP, Hidalgo A. Leukocyte ligands for endothelial selectins: specialized glycoconjugates that mediate rolling and signaling under flow. Blood. 2011;118(26):6743–6751.
   PubMed Web of Science ®Google Scholar
• Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol. 2007;7(9):678–689.
   PubMed Web of Science ®Google Scholar
• Massena S, Christoffersson G, Hjertstrom E, et al. A chemotactic gradient sequestered on endothelial heparan sulfate induces directional intraluminal crawling of neutrophils. Blood. 2010;116(11):1924–1931.
   PubMed Web of Science ®Google Scholar
• BcDonald B, Pittman K, Menezes GB, et al. Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science. 2010;330(6002):362–366.
   PubMed Web of Science ®Google Scholar
• Luster AD, Alon R, Andrian UH. Immune cell migration in inflammation: present and future therapeutic targets. Nat Immunol. 2005;6(12):1182–1190.
   PubMed Web of Science ®Google Scholar
• Sackstein R, Schatton T, Barthel SR. T-lymphocyte homing: an underappreciated yet critical hurdle for successful cancer immunotherapy. Lab Invest. 2017;97(6):669–697.
   PubMed Web of Science ®Google Scholar
• Becker AD, Riet IV. Homing and migration of mesenchymal stromal cells: how to improve the efficacy of cell therapy? World J Stem Cells. 2016;8(3):73–87.
   PubMed Web of Science ®Google Scholar
• None TM, None AC, SH Ranganath. Bioengineered cellular and cell membrane-derived vehicles for actively targeted drug delivery: so near and yet so far. Adv Drug Deliv Rev. 2018;132:57–80.
   PubMed Web of Science ®Google Scholar
• Roger M, Clavreul A, Venier-Julienne MC, et al. Mesenchymal stem cells as cellular vehicles for delivery of nanoparticles to brain tumors. Biomaterials. 2010;31(32):8393–8401.
   PubMed Web of Science ®Google Scholar
• Aleynik A, Gernavage KM, Mourad YS, et al. Stem cell delivery of therapies for brain disorders. Clin Transl Med. 2014;3:24.
   PubMedGoogle Scholar
• Lopez-Santalla M, Hervas-Salcedo R, Fernandez-Garcia M, Bueren JA, Garin MI. Cell therapy with mesenchymal stem cells induces an innate immune memory response that attenuates experimental colitis in the long term. J Crohns Colitis. 2020;14(10):1424–1435.
   PubMed Web of Science ®Google Scholar
• Porada CD, Almeida-Porada G. Mesenchymal stem cells as therapeutics and vehicles for gene and drug delivery. Adv Drug Deliv Rev. 2010;62(12):1156–1166.
   PubMed Web of Science ®Google Scholar
• Höckel M, Vaupel P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst. 2001;93(4):266–276.
   PubMedGoogle Scholar
• Pattabiraman DR, Weinberg RA. Tackling the cancer stem cells - what challenges do they pose? Nat Rev Drug Discov. 2014;13(7):497–512.
   PubMed Web of Science ®Google Scholar
• Winner M, Koong AC, Rendon BE, Zundel W, Mitchell RA. Amplification of tumor hypoxic responses by macrophage migration inhibitory factor-dependent hypoxia-inducible factor stabilization. Cancer Res. 2007;67(1):186–193.
   PubMed Web of Science ®Google Scholar
• Konisti S, Kiriakidis S, Paleolog EM. Hypoxia--A key regulator of angiogenesis and inflammation in rheumatoid arthritis. Nat Rev Rheumatol. 2012;8(3):153–162.
   PubMed Web of Science ®Google Scholar
• Finger EC, Giaccia AJ. Hypoxia, inflammation, and the tumor microenvironment in metastatic disease. Cancer Metastasis Rev. 2010;29(2):285–293.
   PubMed Web of Science ®Google Scholar
• Gregory JL, Morand EF, McKeown SJ, et al. Macrophage migration inhibitory factor induces macrophage recruitment via CC chemokine ligand 2. J Immunol. 2006;177(11):8072–8079.
   PubMed Web of Science ®Google Scholar
• Zlotnik A, Burkhardt AM, Homey B. Homeostatic chemokine receptors and organ-specific metastasis. Nat Rev Immunol. 2011;11(9):597–606.
   PubMed Web of Science ®Google Scholar
• Goswami KK, Ghosh T, Ghosh S, Sarkar M, Bose A, Baral R. Tumor promoting role of anti-tumor macrophages in tumor microenvironment. Cell Immunol. 2017;316:1–10.
   PubMed Web of Science ®Google Scholar
• Yang L, Zhang Y. Tumor-associated macrophages: from basic research to clinical application. J Hematol Oncol. 2017;10(1):58.
   PubMed Web of Science ®Google Scholar
• Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy. Immunity. 2014;41(1):49–61.
   PubMed Web of Science ®Google Scholar
• Spaeth E, Klopp A, Dembinski J, Andreeff M, Marini F. Inflammation and tumor microenvironments: defining the migratory itinerary of mesenchymal stem cells. Gene Ther. 2008;15(10):730–738.
   PubMed Web of Science ®Google Scholar
• Liesveld JL, Sharma N, Aljitawi OS. Stem cell homing: from physiology to therapeutics. Stem Cells. 2020;38(10):1241–1253.
   PubMed Web of Science ®Google Scholar
• Domanska UM, Kruizinga RC, Nagengast WB, et al. A review on CXCR4/CXCL12 axis in oncology: no place to hide. Eur J Cancer. 2013;49(1):219–230.
   PubMed Web of Science ®Google Scholar
• Mukherjee S, Ghosh RN, Maxfield FR. Endocytosis. Physiol Rev. 1997;77(3):759–803.
   PubMed Web of Science ®Google Scholar
• Doherty GJ, McMahon HT. Mechanisms of endocytosis. Annu Rev Biochem. 2009;78:857–902.
   PubMed Web of Science ®Google Scholar
• Gordon S. Phagocytosis: an immunobiologic process. Immunity. 2016;44(3):463–475.
   PubMed Web of Science ®Google Scholar
• Aderem A, Underhill DM. Mechanisms of phagocytosis in macrophages. Annu Rev Immunol. 1999;17(1):593–623.
   PubMed Web of Science ®Google Scholar
• Batrakova EV, Gendelman HE, Kabanov AV. Cell-mediated drug delivery. Expert Opin Drug Deliv. 2011;8(4):415–433.
   PubMed Web of Science ®Google Scholar
• Hillaireau H, Couvreur P. Nanocarriers’ entry into the cell: relevance to drug delivery. Cell Mol Life Sci. 2009;66(17):2873–2896.
   PubMed Web of Science ®Google Scholar
• Lin SY, Hsu WH, Lo JM, Tsai HC, Hsiue GH. Novel geometry type of nanocarriers mitigated the phagocytosis for drug delivery. J Control Release. 2011;154(1):84–92.
   PubMed Web of Science ®Google Scholar
• Champion JA, Katare YK, Mitragotri S. Making polymeric micro- and nanoparticles of complex shapes. Proc Natl Acad Sci U S A. 2007;104(29):11901–11904.
   PubMed Web of Science ®Google Scholar
• Champion JA, Mitragotri S. Role of target geometry in phagocytosis. Proc Natl Acad Sci U S A. 2006;103(13):4930–4934.
   PubMed Web of Science ®Google Scholar
• Gehl J. Electroporation: theory and methods, perspectives for drug delivery, gene therapy and research. Acta Physiol Scand. 2003;177(4):437–447.
   PubMedGoogle Scholar
• Xie Z, Su Y, Kim GB, et al. Immune cell-mediated biodegradable theranostic nanoparticles for melanoma targeting and drug delivery. Small. 2017;13(10):10.
   Web of Science ®Google Scholar
• Lizano C, Sanz S, Luque J, Pinilla M. In vitro study of alcohol dehydrogenase and acetaldehyde dehydrogenase encapsulated into human erythrocytes by an electroporation procedure. Biochim Biophys Acta. 1998;1425(2):328–336.
   PubMed Web of Science ®Google Scholar
• Kim SH, Kim EJ, Hou JH, et al. Opsonized erythrocyte ghosts for liver-targeted delivery of antisense oligodeoxynucleotides. Biomaterials. 2009;30(5):959–967.
   PubMed Web of Science ®Google Scholar
• Chen FG, Wang C, Zhi DY, Xia GM. Analysis of amino acids in individual wheat embryonic protoplast. Amino Acids. 2005;29(3):235–239.
   PubMed Web of Science ®Google Scholar
• Ponsaerts P, Bosch GV, Cools N, et al. Messenger RNA electroporation of human monocytes, followed by rapid in vitro differentiation, leads to highly stimulatory antigen-loaded mature dendritic cells. J Immunol. 2002;169(4):1669–1675.
   PubMed Web of Science ®Google Scholar
• Prechtel AT, Turza NM, Theodoridis AA, Kummer M, Steinkasserer A. Small interfering RNA (siRNA) delivery into monocyte-derived dendritic cells by electroporation. J Immunol Methods. 2006;311(1–2):139–152.
   PubMed Web of Science ®Google Scholar
• He H, Ye J, Wang Y, et al. Cell-penetrating peptides meditated encapsulation of protein therapeutics into intact red blood cells and its application. J Control Release. 2014;176:123–132.
   PubMed Web of Science ®Google Scholar
• López SC, Meissner KE. Characterization of carrier erythrocytes for biosensing applications. J Biomed Opt. 2017;22(9):91510.
   PubMed Web of Science ®Google Scholar
• Sanz S, Lizano C, Luque J, Pinilla M. In vitro and in vivo study of glutamate dehydrogenase encapsulated into mouse erythrocytes by a hypotonic dialysis procedure. Life Sci. 1999;65(26):2781–2789.
   PubMed Web of Science ®Google Scholar
• Hamidi M, Tajerzadeh H. Carrier erythrocytes: an overview. Drug Deliv. 2003;10(1):9–20.
   PubMed Web of Science ®Google Scholar
• Markov DE, Boeve H, Gleich B, et al. Human erythrocytes as nanoparticle carriers for magnetic particle imaging. Phys Med Biol. 2010;55(21):6461–6473.
   PubMed Web of Science ®Google Scholar
• Gao M, Hu A, Sun X, et al. Photosensitizer decorated red blood cells as an ultrasensitive light-responsive drug delivery system. ACS Appl Mater Interfaces. 2017;9(7):5855–5863.
   PubMed Web of Science ®Google Scholar
• Chambers E, Mitragotri S. Prolonged circulation of large polymeric nanoparticles by non-covalent adsorption on erythrocytes. J Control Release. 2004;100(1):111–119.
   PubMed Web of Science ®Google Scholar
• Lee DY, Cha BH, Jung M, Kim AS, Bull DA, Won YW. Cell surface engineering and application in cell delivery to heart diseases. J Biol Eng. 2018;12:28.
   PubMed Web of Science ®Google Scholar
• Yu H, Yang Z, Li F, Xu L, Sun Y. Cell-mediated targeting drugs delivery systems. Drug Deliv. 2020;27(1):1425–1437.
   PubMed Web of Science ®Google Scholar
• Stephan MT, Moon JJ, Um SH, Bershteyn A, Irvine DJ. Therapeutic cell engineering with surface-conjugated synthetic nanoparticles. Nat Med. 2010;16(9):1035–1041.
   PubMed Web of Science ®Google Scholar
• Kim H, Shin K, Park OK, et al. General and facile coating of single cells via mild reduction. J Am Chem Soc. 2018;140(4):1199–1202.
   PubMed Web of Science ®Google Scholar
• Swiston AJ, Cheng C, Um SH, Irvine DJ, Cohen RE, Rubner MF. Surface functionalization of living cells with multilayer patches. Nano Lett. 2008;8(12):4446–4453.
   PubMed Web of Science ®Google Scholar
• Li L, Guan Y, Liu H, et al. Silica nanorattle-doxorubicin-anchored mesenchymal stem cells for tumor-tropic therapy. ACS Nano. 2011;5(9):7462–7470.
   PubMed Web of Science ®Google Scholar
• Parrott MB, Adams KE, Mercier GT, Mok H, Campos SK, Barry MA. Metabolically biotinylated adenovirus for cell targeting, ligand screening, and vector purification. Mol Ther. 2003;8(4):688–700.
   PubMed Web of Science ®Google Scholar
• Thomsen T, Klok HA. Chemical cell surface modification and analysis of nanoparticle-modified living cells. ACS Appl Bio Mater. 2021;4(3):2293–2306.
   PubMedGoogle Scholar
• Cheng H, Kastrup CJ, Ramanathan R, et al. Nanoparticulate cellular patches for cell-mediated tumoritropic delivery. ACS Nano. 2010;4(2):625–631.
   PubMed Web of Science ®Google Scholar
• Yao S, Li X, Liu J, Sun Y, Wang Z, Jiang Y. Maximized nanodrug-loaded mesenchymal stem cells by a dual drug-loaded mode for the systemic treatment of metastatic lung cancer. Drug Deliv. 2017;24(1):1372–1383.
   PubMed Web of Science ®Google Scholar
• Mooney R, Weng Y, Tirughana-Sambandan R, et al. Neural stem cells improve intracranial nanoparticle retention and tumor-selective distribution. Future Oncol. 2014;10(3):401–415.
   PubMed Web of Science ®Google Scholar
• Sakahara H, Saga T. Avidin-biotin system for delivery of diagnostic agents. Adv Drug Deliv Rev. 1999;37(1–3):89–101.
   PubMed Web of Science ®Google Scholar
• Ahmed KK, Geary SM, Salem AK. Surface engineering tumor cells with adjuvant-loaded particles for use as cancer vaccines. J Control Release. 2017;248:1–9.
   PubMed Web of Science ®Google Scholar
• Chinol M, Caslini P, Maggiolo M, et al. Biochemical modifications of avidin improve pharmacokinetics and biodistribution, and reduce immunogenicity. Br J Cancer. 1998;78(2):189–197.
   PubMed Web of Science ®Google Scholar
• Ravasan S, Madadi E, Fathi Z, et al. The effect of Yarrowia lipolytical-asparaginase on apoptosis induction and inhibition of growth in Burkitt’s lymphoma Raji and acute lymphoblastic leukemia MOLT-4 cells. Int J Biol Macromol. 2020;146:193–201.
   PubMed Web of Science ®Google Scholar
• Godfrin Y, Horand F, Franco R, et al. International seminar on the red blood cells as vehicles for drugs. Expert Opin Biol Ther. 2012;12(1):127–133.
   PubMed Web of Science ®Google Scholar
• Galluzzi L, Senovilla L, Vacchelli E, et al. Trial watch: dendritic cell-based interventions for cancer therapy. Oncoimmunology. 2012;1(7):1111–1134.
   PubMed Web of Science ®Google Scholar
• Anassi E, Ndefo UA. Sipuleucel-T (provenge) injection: the first immunotherapy agent (vaccine) for hormone-refractory prostate cancer. P T. 2011;36(4):197–202.
   PubMedGoogle Scholar
• Portnow J, Synold TW, Badie B, et al. Neural stem cell-based anticancer gene therapy: a first-in-human study in recurrent high-grade glioma patients. Clin Cancer Res. 2017;23(12):2951–2960.
   PubMed Web of Science ®Google Scholar
• Portnow J, Badie B, Synold TW, et al. A first-in-human study of neural stem cells (NSCs) expressing cytosine deaminase (CD) in combination with 5-fluorocytosine (5-FC) in patients with recurrent high-grade glioma. J Clin Oncol. 2013;31(15):2018.
   Web of Science ®Google Scholar
• Rossi L, Serafini S, Cenerini L, et al. Erythrocyte-mediated delivery of dexamethasone in patients with chronic obstructive pulmonary disease. Biotechnol Appl Biochem. 2001;33(2):85–89.
   PubMed Web of Science ®Google Scholar
• Kurtzberg J, Prockop S, Teira P, et al. Allogeneic human mesenchymal stem cell therapy (remestemcel-L, Prochymal) as a rescue agent for severe refractory acute graft-versus-host disease in pediatric patients. Biol Blood Marrow Transplant. 2014;20(2):229–235.
   PubMed Web of Science ®Google Scholar
• Beduneau A, Ma Z, Grotepas CB, et al. Facilitated monocyte-macrophage uptake and tissue distribution of superparmagnetic iron-oxide nanoparticles. PLoS One. 2009;4(2):e4343.
   PubMed Web of Science ®Google Scholar
• Sarkar S, Thapa R, Naushin F, et al. Antibiotic-loaded smart platelet: a highly effective invisible mode of killing both antibiotic-sensitive and -resistant bacteria. ACS Omega. 2022;7(28):24102–24110.
   PubMed Web of Science ®Google Scholar
• Choi J, Kim HY, Ju EJ, et al. Use of macrophages to deliver therapeutic and imaging contrast agents to tumors. Biomaterials. 2012;33(16):4195–4203.
   PubMed Web of Science ®Google Scholar
• Lizano C, Pérez MT, Pinilla M. Mouse erythrocytes as carriers for coencapsulated alcohol and aldehyde dehydrogenase obtained by electroporation in vivo survival rate in circulation, organ distribution and ethanol degradation. Life Sci. 2001;68(17):2001–2016.
   PubMed Web of Science ®Google Scholar
• Levene M, Bain MD, Moran NF, et al. Safety and efficacy of erythrocyte encapsulated thymidine phosphorylase in mitochondrial neurogastrointestinal encephalomyopathy. J Clin Med. 2019;8(4):457.
   PubMed Web of Science ®Google Scholar
• Anselmo AC, Gupta V, Zern BJ, et al. Delivering nanoparticles to lungs while avoiding liver and spleen through adsorption on red blood cells. ACS Nano. 2013;7(12):11129–11137.
   PubMed Web of Science ®Google Scholar
• Stephan MT, Stephan SB, Bak P, Chen J, Irvine DJ. Synapse-directed delivery of immunomodulators using T-cell-conjugated nanoparticles. Biomaterials. 2012;33(23):5776–5787.
   PubMed Web of Science ®Google Scholar
• Rossi NA, Constantinescu I, Kainthan RK, Brooks DE, Scott MD, Kizhakkedathu JN. Red blood cell membrane grafting of multi-functional hyperbranched polyglycerols. Biomaterials. 2010;31(14):4167–4178.
   PubMed Web of Science ®Google Scholar
• Yan H, Mi X, Midgley AC, et al. Targeted repair of vascular injury by adipose-derived stem cells modified with P-selectin binding peptide. Adv Sci. 2020;7(11):1903516.
   Web of Science ®Google Scholar
• Xu P, Zuo H, Zhou R, et al. Doxorubicin-loaded platelets conjugated with anti-CD22 mAbs: a novel targeted delivery system for lymphoma treatment with cardiopulmonary avoidance. Oncotarget. 2017;8(35):58322–58337.
   PubMedGoogle Scholar
• Xu M, Asghar S, Dai S, et al. Mesenchymal stem cells-curcumin loaded chitosan nanoparticles hybrid vectors for tumor-tropic therapy. Int J Biol Macromol. 2019;134:1002–1012.
   PubMed Web of Science ®Google Scholar
• Ayer M, Burri O, Guiet R, et al. Biotin-neutravidin mediated immobilization of polymer micro- and nanoparticles on T lymphocytes. Bioconjug Chem. 2021;32(3):541–552.
   PubMed Web of Science ®Google Scholar
• Weiss DJ, Casaburi R, Flannery R, LeRoux-Williams M, Tashkin DP. A placebo-controlled, randomized trial of mesenchymal stem cells in COPD. Chest. 2013;143(6):1590–1598.
   PubMed Web of Science ®Google Scholar